fractures is one of the most important public health issues for the
21st century, as populations across the world grow older and more
prosperous. There are three main approaches to tackling this problem:
drugs, diet and lifestyle. This paper will consider diet and, to a
lesser extent, physical activity and sun exposure.
have focussed almost exclusively on increasing calcium intake. Increasing
calcium intake is not wrong in itself but, in relation to bone health,
its undue pre-eminence over reducing sodium intake, increasing vitamin
K and potassium intakes, moderating protein intake, increasing physical
activity and adequate sun exposure is a serious error in public
There are five
components to promoting bone health through diet:
the ingredients of bone (protein, phosphorus and calcium);
calcium losses from the body;
- making absorption
of calcium from the gut easy;
- making absorption
of calcium from bone difficult;
bone strength independently of bone mass.
the ingredients of bone (protein, phosphorus and calcium)
About 1.0 g
of protein per kg of body weight per day is widely accepted as an
adequate intake for most people over the age of 10, though athletes
may require about 1.5 g per kg per day.
About 1.25 g
of phosphorus per day is also widely accepted as an adequate intake
for most people. Most people in developed countries get adequate
protein and phosphate, though some elderly individuals do not. Elderly
people may need to emphasise foods rich in these nutrients as their
calorie consumption declines.
of 800-1500 mg per day are considered adequate by various expert
bodies. However, calcium requirements cannot be considered separately
from other dietary components, particularly those determining calcium
calcium losses from the body
Calcium is lost
from the body in urine, gut secretions and sweat. The key to avoiding
bone loss is to ensure that calcium absorbed from food in the gut
balances the losses. Otherwise, the body will take calcium from
bone to maintain the required level of calcium in the blood. The
body contains about 1 kg of calcium in the bones. If calcium losses
exceed absorption from the gut by just 30 mg per day, 1% of the
calcium in the bones will be lost each year.
In people following
typical North American and European diets, calcium loss is driven
with approximately equal importance by four dietary components:
high sodium, high protein, low potassium and low bicarbonate intakes.
sodium intake from 1000 to 4000 mg per day causes an additional
52 mg of calcium loss per day.
protein intake from 40 to 100 g per day increases losses by 66
mg per day.
potassium intake from 8000 to 2000 mg per day increases losses
by 31 mg per day.
bicarbonate intake from 100 to 20 mmol per day increases losses
by 32 mg per day.
plausible changes in daily intake of the four key components can
therefore cause calcium losses from the body to increase from about
60 mg per day to about 240 mg per day. Fractional calcium absorption
(the fraction of dietary calcium absorbed from the gut) decreases
as calcium intake increases, so each successive increase in calcium
intake has less effect. For a typical 55 year old woman, the required
calcium intake to meet 60 mg per day of losses would be just 200
mg per day, while the required intake to meet losses of 240 mg per
day would be 2300 mg per day. Appendix 1 explains the calculation
of these figures.
adolescents and younger adults, calcium absorption is more efficient
and adapts better to increased losses. In these groups the beneficial
effect of increasing calcium intake on calcium balance is stronger,
due to better average absorption, and the adverse effect of increased
losses is less, due to better adaptation of absorption to increased
losses. Older men and older women show a decline in absorption (Institute
of Medicine, 1997; Agnusdei, 1998; Barger-Lux, 1995), with average
fractional calcium absorption being about 30-40% lower at eighty
than at thirty. In this briefing paper the analysis will focus on
adults with an average age of about 55. Any diet adequate to support
bone health in older adults will be adequate for younger people,
but in the very old reducing calcium losses will be even more important
than this analysis indicates, as calcium absorption will be lower.
to balance a given calcium loss will also be higher for those with
relatively low calcium absorption for their age. Such individuals
are at particularly high risk of osteoporosis (Need, 1998; Ensrud,
2000). About one in ten postmenopausal women show absorption more
than 40% below the average (Heaney, 1986) and are therefore at particularly
high risk of bone loss. As already noted, the fraction of calcium
absorbed also declines as overall calcium intake increases. A useful
way of examining foods is to evaluate their net impact on calcium
balance (calcium absorbed from the gut minus calcium losses) at
a given level of calcium intake. To fully appreciate the impact
of a food on high risk individuals its effect should be evaluated
with calcium absorption 40% below typical levels.
Table 1 shows
the effect of some representative foods on calcium balance, in mg
of calcium per 100 g of food, at calcium intakes between 500 and
1000 mg per day and between 1000 and 1500 mg per day, both for typical
calcium absorption and for 40% reduced absorption (high risk).
Table 1: Effect of representative foods on calcium balance
Foods can be
categorised based on whether they are high or low in calcium and
whether they increase or decrease calcium losses. The ideal foods
for bone health are foods that are high in calcium and reduce calcium
losses. Adding these foods to the diet will benefit everyone, including
those requiring high calcium intakes and having low absorption.
Green leafy vegetables such as kale and spring greens are the best
example of such foods. In contrast, all dairy foods increase losses
of calcium as well as providing calcium, so their effectiveness
declines dramatically with increased calcium intakes and with decreased
absorption. Foods such as meat, fish and eggs, which are low in
calcium but cause high losses, reduce everyone's calcium balance
uniformly, while low calcium foods which reduce losses, such as
peppers, bananas and oranges, provide everyone with a modest boost.
For an individual
trying to improve calcium balance, fruit and vegetables are the
best foods to add, as they are rich in potassium and bicarbonate
which reduce calcium losses. Adding 100 g of each of the five vegetables
and fruits at the bottom of Table 1 would add 400 mg of calcium
to the diet and 30 to 35 mg to the calcium balance of a high risk
person with low absorption, or 40 to 50 mg for a person with typical
absorption. In contrast, a pint of cow's milk would add about 700
mg of calcium to the diet, but would improve calcium balance by
only 13 to 22 mg and 35 to 50 mg respectively. 100 g of cheddar
cheese would also add 700 mg of calcium to the diet, but would actually
take away 11 to 4 mg of calcium from the high risk person while
adding only 7 to 19 mg to calcium balance for the person with average
risk. In all cases, the benefit is less at higher calcium intakes.
More calcium is a good thing, but the package it comes in is critical,
particularly for individuals at high risk.
protein intake increases calcium losses, an adequate protein intake
is essential to provide the ingredients for muscle and bone, without
which the body will degenerate. Consuming less than the recommended
amount of protein in order to reduce calcium loss is therefore a
false economy. However, the choice of protein source can make a
great deal of difference. A person trying to increase protein intake
using chicken or fish will lose 25 mg of calcium from their body
for every 100 g eaten. In contrast, a 100 g portion of beans (by
dry weight) has an approximately neutral effect on calcium balance
while providing the same amount of protein.
intake by 5 g per day will eliminate 2000 mg of sodium, reducing
calcium losses by about 35 mg per day.
intake; increasing potassium and bicarbonate intake from fruit and
vegetables; meeting protein needs from legumes rather than meat,
fish or egg; and getting calcium from green leafy vegetables rather
than dairy products can reduce the losses of calcium from the body
substantially. As already noted, if calcium losses exceed calcium
absorption by just 30 mg per day about 1% of bone calcium will be
lost each year. Reducing calcium losses while consuming ample calcium
(about 1000 mg per day) provides a robust foundation for bone health
by making it easier for the body to replenish its losses from the
of calcium from the gut easy
Faced with a
given calcium loss, the body will try to maintain calcium levels
in the blood by taking calcium from the gut or from bone. If calcium
is readily available from food in the gut, the body is less likely
to remove it from bone, so bone loss will be less.
The body maintains
blood levels of calcium primarily by adjusting parathyroid hormone
(PTH). Increased PTH increases the production of calcitriol from
calcidiol (stored vitamin D) as well as directly stimulating removal
of calcium from bone. Calcitriol stimulates absorption of calcium
both from the gut and from bone. Calcidiol has similar effects to
calcitriol, though these effects are weaker at normal concentrations.
If calcium intake
is sufficient to meet calcium losses with a low fractional calcium
absorption and vitamin D is adequate, the body will show low PTH,
moderate to high calcidiol and low calcitriol. This combination
favours calcium being taken from the gut rather than from bone and
indicates ideal calcium metabolism.
If vitamin D
is adequate but calcium intake is not ample, the body will show
moderate PTH, moderate to high calcidiol and high calcitriol. This
is undesirable as calcium is likely to be absorbed from bone as
well as from the gut and bone loss may be significant.
If vitamin D
is inadequate, the body will show high PTH, low calcidiol and low
calcitriol. In this case, calcium will be lost from bone. Severely
inadequate vitamin D levels manifest as rickets in children and
as osteomalacia in adults.
deficiency impairs calcium absorption from the gut (Sojka, 1995).
Magnesium is abundant in unrefined plant foods, including whole
absorption of calcium from the gut. One cup of caffeine-containing
coffee per day reduces calcium balance by about 4 mg (Barger-Lux,
1995b). This is a very significant reduction in older adults, leading
to about 0.1% loss of bone per year if not compensated for by some
health requires adequate stored vitamin D (calcidiol) and magnesium
combined with sufficient calcium intake to allow calcium losses
to be met from the gut even with a low fractional absorption.
of calcium from bone difficult
The other side
of ensuring that calcium comes from the gut and not from bone is
making bone resistant to calcium loss. When the body demands more
calcium to balance losses, by raising PTH and calcitriol, both the
gut and the bone will respond. Making it easy to absorb calcium
from the gut helps to protect bone. Helping bone to resist demands
for more calcium is just as important.
Bone is built
by osteoblast cells and demolished by osteoclast cells in an ongoing
cycle of renewal and repair. Strengthening osteoblast activity relative
to osteoclast activity makes bone more resistant to demands for
release of calcium to the blood. Increased resistance means that
more of the calcium losses will be met by absorption from the gut
and less by absorption from bone.
and adolescence, growth hormones strongly stimulate osteoblast activity,
promoting a positive calcium balance. Growth hormones decline with
age. Particularly severe declines in bone growth hormones occur
if dietary protein, phosphate or zinc become inadequate. Oestrogen
levels also decline with age in both men and women, with a particularly
dramatic drop in women at menopause. Oestrogen promotes a positive
calcium balance in many ways, including making bone more resistant
to releasing calcium in response to increased PTH, reducing urinary
calcium loss and possibly increasing calcium absorption (Nordin,
1999; Riggs, 1998). These age-related changes shift the balance
in favour of osteoclast activity with age, making bone loss in response
to calcium losses more likely.
A key component
of bone is osteocalcin, a protein produced by osteoblasts. Osteocalcin
must be carboxylated to bind most effectively with calcium. Elevated
undercarboxylated osteocalcin (ucOC) strongly predicts fracture
risk and is associated with both decreased bone density and weaker
bones at a given density (Weber, 2001). Elevated ucOC can be readily
corrected by increased vitamin K intake. Vitamin K is found in large
quantities in green leafy vegetables and broccoli and in the fermented
soy product, natto. Absorption of vitamin K from green leafy vegetables
is enhanced by the presence of fat, e.g. from a salad dressing,
cooking oil or other accompanying food. Booth (2000) found high
vitamin K intake (250 micrograms per day) to be associated with
a 65% reduction in fracture risk. 250 micrograms of vitamin K can
be obtained from 100 g of broccoli or green cabbage, 200 g of lettuce
or just 40 g of kale (Shearer, 1996). The beneficial effect of vitamin
K is particularly notable in postmenopausal women who are not receiving
oestrogen treatment, suggesting that it counters some of the adverse
effects of declining oestrogen levels (Feskanich, 1999). In those
postmenopausal women showing particularly high calcium losses a
1000 microgram vitamin K supplement resulted in a marked reduction
in urinary calcium losses (Knapen, 1989). A 1000 microgram supplement
is equivalent to about 150 g of kale. Vitamin K may also be important,
together with ample calcium intake, in ensuring a beneficial impact
of increased levels of vitamin D (Feskanich, 1999).
Blood pH is
also a significant factor in osteoblast and osteoclast activity.
As pH drops, the balance is shifted in favour of osteoclasts and
bone density declines (Bushinsky, 2000; Giannini, 1998). Blood pH
decreases with age, as kidney efficiency declines, and is sensitive
to the balance between acid and bicarbonate from the diet (Sebastian,
1994; Frassetto, 1996).
foods (typically high in potassium relative to protein) increases
blood pH, thereby shifting the balance in favour of the osteoblasts.
However, low protein diets have the opposite effect as they cause
a decline in growth hormones. It is therefore very important to
maintain adequate protein intakes while using plenty of alkaline
foods such as fruits and vegetables to balance the acid from the
protein. Vegetable sources of protein (other than grains and some
nuts) are usually alkaline, while animal sources of protein are
usually acid. Milk is approximately neutral, but cheese is even
more acid than meat or fish.
Table 2 shows
the contribution of different types of food to net alkali. For the
detail of the calculation of net alkali see Appendix 1. Acid foods
show a negative value for net alkali.
Table 2: The effect of representative foods on net alkali
probably has an adverse effect in older adults by stimulating release
of calcium from bone and also by interfering with absorption of
calcium from the gut (Binkley, 2000; Johansson, 2001). Major studies
in both Scandinavia and the USA have linked retinol intakes above
1500 micrograms per day with an almost doubled risk of hip fracture
compared with retinol intakes below 500 micrograms per day (Melhus,
1998, Feskanich, 2002). Both studies found that plant carotenes,
from which the body can make its own vitamin A as required, were
not associated with increased risk. Retinol is found in animal products,
particularly liver and cod liver oil. It is also found in some fortified
foods, including most milk sold in Sweden and the USA, and many
multivitamin supplements. Plant carotenes are abundant in carrots,
dark green leafy vegetables and red peppers.
Vitamin C promotes
the formation of osteoblast-derived proteins required in bone.
acids may have a positive effect in shifting the balance in favour
of osteoblasts (Kruger, 1998; Requirand, 2000; Watkins, 2001).
has a huge impact in promoting osteoblast activity, thus encouraging
the body to take the necessary calcium from the gut rather than
the bones. For a given dietary intake, greater physical activity
such as walking, running, racket sports and weight training will
promote the development and retention of bone (Uusi-Rasi, 1998;
Wolff, 1999). In the face of high physical activity, the body will
follow the path of least resistance and take extra calcium from
the gut rather than from bone.
combination is a diet requiring a relatively low fractional absorption
of calcium to balance losses and a combination of physical activity
and dietary factors promoting osteoblast activity so as to make
the bones resistant to the body's demands for calcium.
bone strength independently of bone mass
Bone mass is
not the end of the story. A large, dense bone is usually a strong
bone, but is not necessarily so. As discussed above, increased vitamin
K intake is associated with reduced fracture risk independent of
bone density. Magnesium in bone promotes a fine crystalline structure
and greater bone strength, so ample magnesium intake may enhance
bone strength (Sojka, 1995).
of low oxalate high calcium green leafy vegetables
are not the ideal food for bone health. 100 g of a low oxalate high
calcium green leafy vegetable such as kale, turnip greens or spring
greens (young cabbage without a heart) will have at least as much
beneficial effect on calcium balance as 200 g of milk or 100 g of
cheddar cheese. Using the green stuff instead of the white stuff
avoids the adverse effects of dairy fat on cardiovascular health.
Dark green leafy vegetables will also protect and strengthen bone
by raising blood pH and providing vitamin K and vitamin C. They
are a good source of plant carotenes which meet the body's needs
for vitamin A safely and naturally. Green leafy vegetables are also
high in folate, which is very beneficial to general health. It is
hard to imagine a food more supportive of bone health than kale
or spring greens.
such as spinach, beet greens, purslane, amaranth and rhubarb are
high in oxalate, which hinders absorption of their calcium. Use
of these foods is not harmful to bone, but their effective calcium
content is only about 20% of the measured content.
If you use salt,
substitute one of the widely available low sodium alternatives containing
at least twice as much potassium as sodium by weight. Anyone relying
on iodised salt as a source of iodine should take a 150 microgram
iodine supplement three times a week if the low sodium substitute
does not provide iodine.
Use low sodium
bread or consume bread moderately, as bread is a major source of
sodium. Some low sodium breads are also fortified with calcium.
Use herbs and
spices instead of salt and salty pickles. There are often similar
products in terms of taste with very different salt levels.
Get at least
600 mg of calcium per day from calcium rich foods or supplements
Kale and spring
greens provide about 150 mg of calcium per 100 g raw weight.
and molasses each provide about 250 mg of calcium per 100 g. While
these foods are too concentrated to consume in large amounts, they
can make a useful contribution. These sources of plant calcium also
provide alkali to boost blood pH. In contrast, milk is neutral and
cheese is acid.
Tofu is high
in calcium only if calcium has been used in preparing it. Some tofu
is highly salted. Tofu can therefore vary from substantially increasing
calcium balance to substantially decreasing it. The calcium content
of tahini is also very variable, ranging from 140 to 960 mg per
100 g. The amounts of calcium and sodium in these foods should be
checked on the labels and not taken for granted. There should be
at least as much calcium as sodium for a beneficial effect on calcium
foods or calcium supplements provide another source of calcium.
Calcium supplements are at least as natural as dairy products or
soy products as humans have consumed calcium carbonate, introduced
via stone grinding of grain, for about 10,000 years. If phosphate
intakes are low (unusual for vegans), calcium phosphate may be preferable
to calcium carbonate or calcium citrate. Calcium carbonate should
always be consumed with meals. If stomach acid is low something
other than carbonate should be used.
600 mg of calcium
per day from calcium rich foods, plus calcium from other foods,
should give an adequate calcium intake.
Get an adequate
This is mainly
an issue for elderly people and others with a relatively low calorie
intake (less than 30 kcal per kg of body weight), but can be of
critical importance. If protein intake is inadequate, the body lacks
the building blocks for muscle and bone, and growth hormones which
stimulate muscle and bone building will decline to undesirable levels.
A cup (250 ml) of soya milk a day provides about 8g of protein and
can make a significant contribution to maintaining an adequate protein
intake. Most dry beans contain about 25 g of protein per 100 g.
Wheat is higher in protein than rice and potatoes, and using nuts
and seeds rather than oils and fats will boost protein intake. Nuts
which are high in monounsaturated fat, such as almonds, hazelnuts
(filberts) and cashews, are ideal as they will also promote cardiovascular
health. Almonds are the most beneficial for bone health as they
have the most positive effect on calcium balance.
an adequate store of vitamin D
short exposures of skin to sun whenever the sun is at least 30 degrees
above the horizon. At latitudes above about 50 degrees North, this
is not practical from November to March, and vitamin D stores will
decay substantially during this "vitamin D winter". Within
30 degrees of the equator there is no vitamin D winter. A fifteen
minute exposure to sun is ample to boost vitamin D while avoiding
For the part
of the year when such sun exposure is not possible, do one of the
- take a mid-winter
holiday somewhere sunny and expose skin to sun frequently;
- use a sunlamp
with at least 3% of its energy between 290 nanometres and 315
nanometres once a week, being careful to avoid overexposure;
- take 10 micrograms
of vitamin D2 (ergocalciferol) per day.
plant foods your main source of protein
Legume and dairy
proteins have a lower sulphur amino acid content (the active component
in causing calcium loss) per gram of protein than meat, fish, egg
or grain proteins, and therefore cause less calcium loss for a given
protein intake. Meat, fish and eggs have a pronounced negative effect
on calcium balance. Grains have a moderately negative effect. Some
highly processed plant protein sources, such as certain soy protein
isolates, have an adverse effect on calcium balance due to loss
of beneficial minerals and addition of sodium during processing.
Highly salted nuts also have an adverse effect. Of the animal protein
sources, only milk and yoghurt can be expected to have a consistently
positive effect on calcium balance. Most plant protein sources (fruits,
vegetables, legumes and many nuts and seeds) come in a nutritional
package which has a positive or neutral effect on calcium balance.
foods are also excellent sources of magnesium.
of vegetables and fruit
fruit promote bone health by improving calcium balance, providing
plentiful vitamin C, and raising blood pH. Several recent studies
have shown that increased fruit and vegetable intake is associated
with increased bone mineral density and decreased loss of bone (Tucker,
1999; New, 2000).
fatty acids in your diet
promote osteoblast (bone-building) activity. The simplest way for
vegans to top up omega-3s is to consume 1-2 teaspoons of flaxseed
oil per day.
been shown to reduce calcium absorption. Low caffeine teas, such
as Redbush (Rooibosch), provide a tasty and healthful alternative.
vitamin A from plant carotenes, not from retinol
the body to regulate production of vitamin A and avoids the probable
ill effects of retinol on bone. Note that cow's milk is fortified
with retinol in Sweden, the USA and some other countries. Some vegan
supplements contain retinol or related compounds - ingredients beginning
with "retin" should be avoided. Good sources of plant
carotenes include carrots, pumpkin, sweet potato, dark green leafy
vegetables, such as kale, spring greens and spinach, and red peppers.
100 grams per day of any combination of these will meet vitamin
A requirements safely and naturally.
don't forget physical activity: just as exercise helps to build
and maintain muscle, it also helps to build and maintain bone
on any health issue need to be consistent with overall health.
and calcium intakes and reduced sodium intake strongly promote lower
blood pressure and reduced risk of stroke and kidney disease.
or vitamin D appears to reduce risk of colorectal cancer and may
also reduce risk of breast cancer. Increased vitamin D may also
reduce the risk of prostate cancer and auto-immune diseases.
is a consistent association between increased milk consumption and
increased risk of prostate cancer. Giovannucci (1998) suggested
that this association may reflect, at least in part, an adverse
effect of calcium. The main evidence for this suggestion was that
high use of calcium from supplements (more than 900 mg per day)
was associated with an increased risk of prostate cancer even at
moderate intakes of dietary calcium. Use of calcium supplements
providing 1-900 mg per day, with dietary calcium intakes below 1000
mg per day, was associated with a very modest decrease in risk which
may have been due to chance. Looking at combined dietary and supplementary
calcium, a significant increase in risk (200% greater than for low
calcium intakes) was observed only for total calcium intakes above
2000 mg per day. As discussed in Appendix 2, calcium intakes above
2000 mg may have adverse effects even from the point of view of
bone health. The recommendations in this paper aim for a calcium
intake of about 1000 mg, so the results of Giovannucci give no cause
The Vegan Society
briefing paper on Milk and Breast Cancer, produced in November 2001,
provides further information on milk and cancer ( www.vegansociety.com/briefings/milkbreastcancer.htm
of foods rich in plant carotenes is associated with reduced risk
of omega-3 fatty acids, particularly from plant sources, is strongly
associated with reduced risk of heart disease. Omega-3 fatty acids
may also reduce risk of depression and schizophrenia.
of unrefined plant foods, particularly fruit and vegetables, nuts,
seeds and whole grains, is associated with wide-ranging health benefits
and can be expected to promote a longer and healthier life.
errors in public policy on bone health
Having set out
the basis of bone health, it is appropriate to reflect on public
The first serious
error in public policy is the undeserved pre-eminence accorded to
calcium in relation to bone health. Calcium is a very good thing,
but increasing calcium intake from 500 mg per day to 1500 mg per
day will add less than 90 mg per day to the calcium balance of most
older adults, and less than 50 mg per day to the calcium balance
of many such adults. 10 g of salt per day will take about 70 mg
per day away from calcium balance. 4000 mg of extra potassium from
a diet rich in vegetables, fruits and other unrefined plant foods
will add 60 mg per day to calcium balance. At the same time, the
alkali from such foods will help bone keep its calcium where it
belongs. Vitamin K from green leafy vegetables and broccoli will
do the same and promote stronger bones at the same time.
The second serious
error is equating calcium with dairy products. Dairy products are
not the best source of calcium as they promote calcium losses at
the same time as increasing calcium intake. This is particularly
true of cheese, which will degrade the calcium balance of individuals
most at risk of osteoporosis: the very old and people with relatively
poor absorption of calcium. In terms of bone health, dairy products
fortified with retinol are a poisoned offering.
provides a particularly clear illustration of the current tendency
to equate calcium with dairy:
antidairy groups are forced logically to take an anticalcium stance
(not just an antidairy stance). Since in the diets of the industrialized
nations 65-80% of calcium intake comes from dairy products to
be against dairy forces one to be against calcium.
Yet in the same
article Heaney states:
It is now
fairly generally accepted that the diets of evolving hominids
exhibited high calcium densities. Both nonhuman primates today
and contemporary hunter-gatherer peoples regularly consume diets
with calcium densities above 2 mmol/100 kcal [2000 mg per day].
Much of this calcium would have come from vegetable sources
In fact, the
most authoritative source (Eaton, 1991) states that about 90% of
that high calcium intake came from plants. A high intake of vegetables,
fruits, roots and flowers also provided abundant potassium, alkali,
magnesium, vitamin K and vitamin C, all in quantities far above
modern norms. Salt was notably absent.
science is in its infancy with regard to the interactions between
these nutrients, but it is clear that all of them, not just calcium,
contribute to bone health and other aspects of health. While many
modern cultivated foods are sadly much less rich in calcium than
the wild plants with which we evolved, green leafy vegetables are
an exception and therefore of particular importance for modern humans.
Human use of
dairy products is a recent and unnecessary development. A diet rich
in vegetables, fruits and root crops provides the best path back
to healthy bones.
to this paper provide important supporting material.
Appendix 1 sets
out the model used for evaluating calcium balance. This is a novel
synthesis of research results over the past twenty years. This appendix
underpins the conclusions of the paper.
Appendix 2 reviews
the evidence from long term supplementation trials with calcium
or vitamin D and concludes that the evidence for a beneficial effect
on bone health from increased calcium intakes, not exceeding 2000
mg per day, is very strong. This review provides additional support
for the recommendations to include at least 600 mg per day of calcium
from calcium-rich foods or supplements and to ensure an adequate
store of vitamin D.
Appendix 3 reviews
the results of prospective epidemiological studies on dietary calcium
and bone health, with particular emphasis on Feskanich (1997, 1998)
as these studies have been the subject of recent controversy. This
review concludes that findings of increased fracture risk with increased
dietary (dairy) calcium intake in these studies, in contrast to
Holbrook (1988), reflects
- the high
retinol content of low fat milk in the USA;
of the results due to people at high risk of osteoporosis consuming
more dairy products;
use of cheese compared with milk.
The review in
Appendix 3 also confirms that there is no reliable evidence indicating
an adverse effect of calcium in itself on bone health, at least
at intakes below 2000 mg per day. Overall, epidemiological studies
of dairy calcium are consistent with a protective effect in childhood
and adolescence which declines with age and may be reversed in older
adults, particularly in relation to cheese and to dairy products
fortified with retinol.
Appendix 4 reviews
the controversy over protein. This review concludes that there is
real advantage in using vegetable protein sources (except grains)
rather than animal protein sources (except milk and yoghurt) to
ensure an adequate protein intake.
1: A model for calcium balance
Many of the
elements of calcium balance are well known.
Each extra mmol
of sodium in the urine is associated with 0.01 extra mmol of calcium
in the urine (Massey, 1996). About 95% of dietary sodium is excreted
in the urine. Short term metabolic loading studies tend to show
a slightly weaker effect, and cross-sectional studies of free-living
populations tend to show a slightly stronger effect. A recent large
cross-sectional study (Ho, 2001) found a coefficient of 0.014 rather
than 0.01. Overall, a robust approximation is given by
= 0.01 * DNa (mmol)
where DUCa is
the change in urinary calcium and DNa is the change in dietary sodium.
The effect of
protein intake on urinary calcium loss is also well established
(Barzel, 1998; Heaney, 1998; Weaver, 1999). The effect is proportional
to the sulphur content of cysteine and methionine in the diet (though
not to the sulphur content of taurine, which is often excreted intact)
and is equivalent to about 0.1 mmol of urinary calcium loss for
each mmol of sulphur (S) consumed in the diet in the form of methionine
or cysteine. That is
= 0.1 * S (mmol)
cysteine (g)* 8.3 + methionine (g) * 6.7
confirms that this effect is seen in cross-sectional studies as
well as short term loading studies, with an observed calcium loss
of 0.85 mg per gram of protein. As each gram of protein in a typical
diet contributes about 0.275 mmol of sulphur, the predicted effect
of a gram of protein would be 0.0275 mmol (1.1 mg) of calcium. The
short term studies appear to capture a persistent effect.
At this point
consensus fades. Some authors consider the effect of sulphur to
be due to the acid created when sulphur-containing amino acids are
metabolised (2 mmol of acid for each mmol of sulphate). This is
made more plausible by the observation that adding potassium bicarbonate
(KHCO3) to the diet causes a decrease in the excretion of calcium
in the urine. However, the extent of the decrease should be 0.05
mmol of calcium per mmol of bicarbonate if both effects are operating
through the mechanism of net acid excretion. Lemann (1993) provides
a very pertinent summary of short term metabolic loading tests:
= -0.015 * DKHCO3 (mmol)
= 0.0 * DNaHCO3 (mmol)
= -0.005 * DKCl (mmol)
relationships can be combined with the effect of sodium (1) and
rearranged to give an equivalent set of equations in terms of the
effects of individual ions:
= -0.005 * DK (mmol)
= 0.0 * DCl (mmol)
= 0.01 * DNa (mmol)
= -0.01 * DHCO3 (mmol)
It is striking
that the effect of bicarbonate is only -0.01 mmol/mmol while the
effect implied if the influence of protein is mediated by acid is
-0.05 mmol/mmol. This counts strongly against the claim that the
effect of protein is governed by the associated acid, and indicates
that sulphate and bicarbonate effects need to be modelled separately.
observes an effect of urinary potassium, provided by the addition
of potassium bicarbonate to the diet, on urinary calcium of -0.022
mmol/mmol. This is only slightly greater than that indicated by
equation 4, particularly when we note the absorption of dietary
potassium to be about 90%, giving an expected effect of about -0.017.
This observation therefore supports the model above. Sebastian (1994)
also notes that earlier work found a reduction in urinary calcium
by potassium citrate but not by sodium citrate. As citrate is metabolised
in the body equivalently to bicarbonate, this observation is also
consistent with the above model.
provides data on the effect of varying intakes of cysteine and methionine
on urinary calcium losses. Intakes of most minerals are kept approximately
constant between the different test diets, but there is an 8 mmol
per day decrease in potassium between the soy protein and animal
protein diets as well as a 10 mmol per day increase in sulphate
from protein. From the model, the sulphate increase should cause
a 40 mg increase in calcium excretion and the potassium decrease
should cause a 5 mg increase in calcium excretion (if associated
with bicarbonate). The predicted increase of 45 mg per day in urinary
calcium matches the observed increase of 47 mg per day well.
Ho (2001) estimates
the effect of urinary potassium (about 90% of dietary potassium)
on urinary calcium in a free-living population to be
= -0.012 * DUK (mmol)
exceeds the predicted effect for potassium alone (-0.005), but the
effective provision of bicarbonate from the diet is governed by
an ion balance:
is adapted from Remer (1994, 1995) with the substitution of slightly
different estimates for the fractional absorption of potassium (0.9),
magnesium (0.4), calcium (see below) and phosphorus (0.65). All
quantities are in mmol. Phosphorus is denoted by P and magnesium
by Mg. It should be noted that the term bicarbonate is used to represent
any salt that will act as a source of alkali in the body. The effect
of a food on net alkali in the body can be calculated by subtracting
twice the sulphur (equation 3) from the bicarbonate (equation 12).
In typical modern
diets, sodium and chloride are approximately equal and the dominant
factor in providing base is potassium, though its effect is modified
(slightly attenuated) by correlations with other ions in the diet,
particularly phosphate. This means that in practice potassium acts
as an approximate proxy for bicarbonate as well as in its own right.
The earlier equations for the effect of potassium (7) and bicarbonate
(10) therefore predict that the apparent effect of dietary potassium
on urinary calcium will be close to -0.015 mmol urinary calcium
per mmol dietary potassium (the sum of the potassium and bicarbonate
effects), which is consistent with equation 11.
Ho (2001) failed
to find an effect of dietary protein, evaluated by a food frequency
questionnaire, on urinary calcium excretion. This is unsurprising,
as the estimated protein intake will be much less accurate than
the measures of urinary sodium and potassium. In contrast, Heaney
(1998, 2000) used chemically analysed diets and did find such an
bicarbonate and protein have not been found to affect either gut
losses of calcium or losses of calcium in sweat, so the effect on
urinary loss of calcium appears to be the net effect on calcium
losses from the body. This is in contrast to phosphorus which decreases
urinary losses while increasing gut losses, giving no overall effect
on calcium loss (Heaney, 1994).
the model, the dependence of calcium absorption on dietary calcium
intake needs to be quantified. The fractional absorption of calcium
from a single portion (load) of dairy products is given by Weaver
Fraction Absorbed = 0.89 - 0.096 * ln(calcium in portion in
a strong decline in absorption with calcium intake, in a given meal,
but does not lend itself to direct application to calculating the
expected absorption for a given daily intake of calcium. Heaney
(2000) notes that the average fractional absorption is given by
Fraction Absorbed = 0.22 * (daily calcium in grams) ^ (-0.44)
intake to constitute a single load, equations 13 and 14 are very
consistent for calcium intakes above 500 mg per day. This indicates
that the decline in absorption reflects primarily a short term load
effect rather than a longer term adaptation to dietary calcium intake
or to calcium losses.
presents similar relationships, but with slightly lower absorption
at moderate intakes and a more rapid decline in absorption with
intake: 0.18* (daily calcium in grams) ^ (-0.6) for men, and 0.155*
(daily calcium in grams) ^ (-0.66) for women. Agnusdei (1998) indicates
a fractional absorption of 0.19* (daily calcium in grams)^(-0.54).
This paper will use equation 14, but it should be noted that this
choice may somewhat overestimate calcium absorption, particularly
at high intakes.
calcium intake increases so do urinary losses of calcium and endogenous
faecal losses (loss of calcium from the gut without reabsorption).
This means that the net absorption of calcium is less than indicated
above. Recker (1977) examines the effect of calcium carbonate supplementation
on calcium balance in women with an average age of 57. Calcium balance
rises by 72 mg, while calcium absorption rises by 108 mg, as calcium
intake goes from 530 mg to 1480 mg. The expected absorption for
the change in intake is 220 * (1.48 ^0.56 - 0.53^0.56), that is
120 mg. This prediction is a good match to the observed absorption
of 108 mg. However, about a third of the absorbed calcium disappears
as increased losses reduce net absorption by one third compared
to gross absorption.
It would be
preferable to have data from a number of different calcium supplementation
trials to verify the estimate that one third of absorbed calcium
disappears in extra losses, but such data do not seem to be available.
Other sources of evidence do not allow a better model of calcium
dependent losses, though they do indicate that the scale of the
losses is at least as a third of absorbed calcium. Correlation studies
of urinary calcium loss and dietary calcium intake suggest that
about 6 mg of calcium is lost in the urine per 100 mg of calcium
intake (Heaney, 1999). This observed loss will reflect a combination
of the actual effect of calcium on urinary losses and the effect
of associated nutrients in dairy foods, which are accounted for
separately in the model above. This value for calcium-dependent
losses may also overestimate losses at higher calcium intakes, since
losses can be expected to decrease as fractional absorption decreases
with increasing calcium intake. Heaney (1994) provides a relationship
between absorption fraction and endogenous faecal losses. Examining
this relationship shows that these gut losses amount to about 10%
of absorbed calcium for calcium intakes between 500 mg and 1500
mg. This indicates that the dominant calcium-dependent loss is the
urinary loss. Both Heaney (1986) and Heaney (1999) indicate that
a simple straight line relationship between absorbed calcium and
urinary calcium explains a high proportion of the variation in urinary
losses, but neither paper states the slope of the fitted line. Even
if the slope were given, it would be influenced by associated nutrients
as well as by calcium itself. The available data do not justify
a more precise model than assuming that calcium-dependent losses
are a constant proportion of the absorbed calcium and estimating
this proportion from the results of Recker (1977) to be one third.
equation will therefore be used to define the typical absorbed fraction
of calcium, while the increased losses associated with absorbed
calcium will be ignored in calculating the calcium losses.
fraction absorbed = 0.15 * (daily calcium in grams) ^ (-0.44)
daily calcium intake is not known, as in the examination of the
effects of individual foods on calcium balance, the effect on balance
will be evaluated for several different ranges of calcium intake.
For example, for an intake range of 500 mg to 1000 mg, the effective
absorption can be estimated as 0.15 * (1^0.56 - 0.5^0.56) / 0.5,
so 0.096 is the expected net fractional absorption.
The final element
for computing the calcium balance is an estimate of calcium losses
when all dietary drivers (calcium, sodium, potassium, protein and
bicarbonate) are zero. Trial and error comparison with known variations
in total calcium losses indicates 2.0 mmol (80 mg) per day to be
expression for the calcium balance is therefore
(mg) = Ca (mg) * FA - 80 + 40 * (0.005 * K + 0.01 * HCO3 - 0.01 *
* (8.3 * cysteine (g) + 6.7 * methionine (g) ) )
where FA is
the net fractional absorption of dietary calcium and HCO3 is calculated
from equation 12. All quantities are in mmol unless otherwise stated.
If data on cysteine or methionine are missing, but data on protein
are available, then sulphur from protein, in mmol, can be estimated,
based on a typical methionine and cysteine content of protein, as
0.275 * protein (g), instead of using equation 3.
can be used in several ways:
- The effect
of individual foods on calcium balance can be evaluated by assuming
an appropriate net fractional absorption (FA) for the range of
calcium intakes being considered and evaluating the change in
calcium balance due to the mineral and amino acid content of the
- For a given
dietary composition, the predicted overall calcium balance at
typical net fractional absorption (equation 15) can be calculated.
- The required
calcium intake to give calcium balance at typical calcium absorption
can be calculated, keeping other nutrients constant.
- The required
fractional absorption (RFA) to achieve calcium balance can be
calculated by finding the fractional absorption which gives a
zero calcium balance.
- The RFA can
be divided by the typical fractional absorption from equation
15 to give a normalised required fractional absorption (NRFA).
The NRFA provides
a direct measure of how well the overall diet supports bone health.
The lower the NRFA, the better the diet. As variations of more than
a factor of 2 around the absorption predicted from equation 14 are
unusual (Heaney, 1986; Heaney, 2000), an NRFA below 0.5 can be considered
an excellent assurance of bone health, while an NRFA above 2 indicates
a seriously deficient diet.
can be illustrated by examining four example diets: a typical Western
omnivore diet, an estimated palaeolithic diet, a typical Western
vegan diet, and the diet recommended in the overview. All the diets
are based on a 70 kg person consuming 2500 kcal per day. Table 3
also shows the net alkali contribution of the diet as the difference
between the estimated intake of bicarbonate (equation 12) and the
intake of acid from protein. 80% protein absorption is assumed,
with acid equal to twice the sulphur content of the absorbed protein.
here to enlarge table]
Table 3: Diet types, net alkali and calcium balance
omnivore diet has the highest NRFA and the highest calcium loss.
The typical vegan diet and the palaeolithic diet have similar calcium
losses, but because of the higher calcium content in the palaeolithic
diet it would be easier to achieve balance by adaptation mechanisms
increasing the fractional absorption. In contrast, the recommended
diet can maintain calcium balance with fractional absorption below
sheds an interesting light on how our palaeolithic ancestors maintained
healthy bones while consuming large quantities of protein. Despite
a calcium to protein ratio (mg per g) of just 7.5, they are closer
than either typical modern omnivores or vegans to having an adequate
diet to support bone health. Also, the level of base in their diet
adequately counters the acidifying effects of the high protein intake,
so blood and urine pH would not be expected to be low by Western
standards. With high levels of physical activity and sun exposure,
it is likely that they had better calcium absorption than is now
typical, further improving bone health. Interestingly, Eaton (1991)
shows that almost all of the palaeolithic calcium intake came from
plant sources. Unfortunately, with the exception of green leafy
vegetables, the calcium content of cultivated fruits and vegetables
is often much inferior to that of their wild counterparts (Milton,
1999), so vegans need to take some care in their dietary choices
to get sufficient calcium, despite exclusive use of plant foods.
absorption follows equation 15, the required calcium intake to bring
each diet into balance is 2000 mg (omnivore), 2300 mg (palaeolithic),
1200 mg (vegan) and 735 mg (recommended). The corresponding required
calcium to protein ratios of the four diets are 20, 11.5, 24 and
10.5. Heaney (1998) suggests that a calcium to protein ratio of
20 is adequate for bone health. While calcium intake and protein
intake are two of the strongest influences on calcium balance, they
should not be considered in isolation from sodium, potassium and
health points towards increasing calcium and potassium intakes,
moderating protein intake and substantially decreasing sodium intake,
compared with Western standards. This combined strategy has a much
better chance of success than the current (correct but unbalanced)
emphasis on calcium as it is less vulnerable to poor calcium absorption.
of the model to specific foods
calcium balances for the food tables provided in this paper, food
composition data were taken from USDA (1999).
in plants was adjusted where good data were available. The available
calcium in high oxalate plants (spinach, rhubarb, Swiss chard) was
reduced by 80% compared with their nominal content (Weaver, 1997).
Kale, broccoli and Chinese cabbage had available calcium increased
by 10% (Weaver, 1997; Benway 1993, Weaver, 1999). Soy products had
their calcium bioavailability reduced by 25%, while other beans
had their bioavailability reduced by 50% (Weaver, 1993). The bioavailability
of calcium from other foods was not adjusted. The impact on the
calcium balance calculations was substantial for the high oxalate
As the USDA
database does not have data on chloride content, a correction was
made by estimating the excess of chloride over sodium based on McCance
and Widdowson (1991). This adjustment was most significant for meat
and fish, for which it increased the net alkali by 1.5 mmol per
100 g. For whole grains, particularly brown rice, and for bananas,
it decreased the net alkali significantly. The impact on the calcium
balance calculations was negligible.
of the model
The key test
of this model is its ability to predict the effects of specific
One of the most
thorough studies of the effect of milk supplementation is Recker
(1985). This study examined the effect on calcium balance of adding
24 oz (670g) of milk to the diet of 13 postmenopausal women. Calcium
balance was measured one year after supplementation commenced and
compared with control subjects who did not receive extra milk. The
one year interval is vital, as it allows the bone remodelling transient
to decay and the body's adaptation mechanisms to operate, so the
measured balance should reflect the long term effect (Heaney, 2001).
Calcium intake increased from 680 mg per day to 1470 mg per day.
The observed effect on calcium balance was an improvement of 45
mg per day. Using the model in Appendix 1, the predicted effect
on calcium balance of an extra 670 g of cow's milk, starting from
an initial intake of 680 mg per day, is 48 mg per day - a very good
match. If the change in calcium intake had been accomplished using
calcium carbonate, the predicted change in balance would have been
65 mg. The difference reflects the losses associated with the milk
and confirms the validity of the model for predicting the effect
of dairy products on calcium balance.
It is also noteworthy
that after allowance for calcium losses in sweat (about 50 mg per
day), which were not considered in this study, the extra milk changed
the overall calcium balance from a loss of 110 mg per day to a loss
of 65 mg per day. Therefore this study shows that increased calcium
consumption from dairy products up to the highest recommended intake
fails to prevent a net loss of calcium in postmenopausal women.
Nonetheless, the 40% reduction in loss observed is a major improvement.
study is Devine (1995). This study used supplementation of either
calcium lactate gluconate or powdered milk to increase calcium intakes
by about 1000 mg per day in two thirds of the study group. The study
then examined changes in bone mineral density over two years. It
would have been preferable to start the bone mineral density measurements
after one year to avoid the remodelling transient, as the remodelling
transient will increase the apparent effect of increased calcium
intake beyond what would be sustained after the transient has passed.
Calcium intake was estimated from dietary records and sodium intake
from urinary sodium excretion. Models were then developed by statistical
regression for the effects of calcium, sodium and weight on the
change in bone mineral density at different parts of the skeleton.
At two bone sites both calcium and sodium were found to have a statistically
significant effect on rate of change of bone mineral density, with
the effect of 100 mg of calcium being positive and about two times
larger than the negative effect of 100 mg sodium.
effect of milk at the median calcium intake of 1500 mg is about
5.5 mg per 100 g of milk, or 4.6 mg per 100 mg of milk calcium.
The expected effect of the calcium supplement is about 7 mg per
100 mg of calcium. The predicted average effect of calcium intake
on calcium balance is therefore an increase of 5.8 mg per 100 mg.
The expected effect of sodium on calcium balance is a decrease of
1.7 mg per 100 mg. The predicted relative effect of calcium and
sodium is therefore 3.4:1, compared with the observed relative effect
of about 2:1. This suggests that the model is giving a useful prediction
of the observed effect but may be underestimating the adverse effect
of sodium relative to the beneficial effect of calcium. If we took
the coefficient for the effect of sodium from Ho (2001), the predicted
effect of 100 mg of sodium on calcium balance would become a decrease
of 2.4 mg calcium per 100 mg sodium, making the expected relative
degree of consistency between the model and the observations is
argues that increased losses are of limited importance when calcium
intakes are high, as the body will successfully increase calcium
absorption from the gut to compensate for increased losses. There
is some truth in this, in that the body can balance increased losses
by absorbing more calcium from the gut or by absorbing more calcium
from bone. However, the success of the model above in predicting
the results of Recker (1985), indicates that the ability to compensate
for increased losses by increased absorption of calcium from the
gut is limited in post-menopausal women and that increased losses
due to components of milk other than calcium are still reflected
directly in reduced balance after a year of adaptation. As noted
in Recker (1985), "examination of the correlation between protein
intake and calcium balance with calcium intake held constant showed
a reasonably strong negative correlation". Increased protein
intake was also associated with increased bone resorption after
adjustment for calcium intake. At least for postmenopausal women,
the degree of adaptation appears to be limited, even at high calcium
intakes, and the model's predictions of the net effect of foods
on calcium balance appear to be valid.
2: The results of long term trials on calcium supplementation
evidence for the effect of diet on health comes from investigator-controlled
intervention studies of sufficient duration to allow the full effect
of the dietary change to be observed. The fundamental advantage
of such studies is that the results are not distorted (confounded)
by associations between individual dietary choices and other characteristics.
However, most intervention trials on calcium supplementation, either
with supplements or with dairy products, are of such short duration
as to be virtually meaningless.
intake increases substantially the level of PTH in the blood drops
substantially. This reduces the rate of creation of new sites for
bone remodelling - removal of bone by osteoclasts and its replacement
by osteoblasts. However, existing sites continue to be remodelled.
This creates a transient imbalance between osteoclast activity starting
at new sites and osteoblast activity continuing at old sites. The
net result is an increase in bone mass over a period ranging from
6 months in children to 18 months in elderly adults. If supplementation
is stopped, this transient is reversed. If supplementation is continued
beyond the duration of the bone remodelling transient, we see the
underlying long term effect of the supplementation.
Trials of sufficient
duration to see the long term effect of supplementation on bone
density, particularly if they also assess impact on fracture incidence,
provide the strongest evidence for the effect of calcium on bone
health. The handful of trials satisfying this criterion are reviewed
the effect of supplementation on changes in bone density relative
to changes in unsupplemented (control) subjects, the rate of change
in bone mineral density in the supplemented subjects will be calculated
between two years after the start of the trial and the end of the
trial. The rate of change in the control subjects will be calculated
over the entire trial duration.
There have been
three trials of supplementation of calcium, without vitamin D, lasting
for four years and reporting detailed BMD changes in each year of
the study. The rates of change of BMD at various bone sites are
summarised below. For Riggs (1998b) only the rate of change of the
supplemented group relative to the control group can be reported.
here to enlarge table]
Table 4: Results of long term calcium supplementation trials
from Reid (1995) and Peacock (2000) are impressive. Both show a
notable reduction in rate of bone loss. This reduction is consistent
with the estimated 40% improvement in calcium balance observed in
Recker (1985) on making a similar shift in calcium intake using
milk and the estimated 50% improvement in calcium balance observed
by Recker (1977) using calcium carbonate. Reid shows a statistically
significant reduction in fracture risk. Peacock shows a non-significant
reduction in fracture risk. Recker (1996) also carried out a four
year supplementation trial increasing calcium intake from 450 mg
per day to 1650 mg per day using calcium carbonate. This trial did
not report detailed BMD changes year by year, but did report a significant
reduction in fracture incidence in women with a history of vertebral
fractures (7% per year compared with 13% per year). This adds up
to a powerful case for improved bone health with calcium supplementation.
Riggs (1998b) shows no benefit and indeed shows a notable loss of
BMD in the spine in the supplemented group compared with the non-supplemented
group over the last two years of the study. Riggs (1998b) showed
gains in BMD of between 1% and 2.5% at the different bone sites
over the first two years of the study. The contrast between the
first two years and the second two years show that eliminating the
bone remodelling transient is vital in any analysis of the effect
of a treatment on bone health.
There were differences
in the forms of supplements used. Riggs used citrate, Peacock used
citrate malate and Reid and Recker used carbonate. This seems unlikely
to account for the differences in results. The only other obvious
difference is that the supplemented calcium intake in Riggs was
higher than in any other study. It is possible that very high calcium
intakes have adverse effects. For example, calcium intakes above
2000 mg per day combined with high phosphate intakes could disrupt
magnesium absorption (Hardwick, 1990). In Riggs (1998b), a third
of those receiving supplements exhibited greatly increased losses
of calcium in the urine requiring reduction of the supplement dose,
indicating that calcium intake was being pushed beyond desirable
levels. Overall, the lesson from Riggs (1998b) appears to be that
calcium intakes beyond 2000 mg per day should not be encouraged.
The observation that many primates have much higher calcium intakes
relative to body size than a human consuming 2000 mg per day does
not provide assurance of safety as these primates consume high levels
of calcium in the context of a diet rich in other minerals, including
magnesium and potassium (Milton, 1999).
have also been reduced using combined calcium and vitamin D supplementation
(Chapuy, 1992; Chapuy, 1994; Dawson-Hughes, 1997). Chapuy (1992,1994)
supplemented 1.2 g of calcium, as calcium phosphate, and 20 micrograms
of vitamin D3 on top of a dietary calcium intake of 500 mg per day
and initial calcidiol levels of about 40 nmol/l. Fracture rate was
reduced by 25% over three years. Dawson-Hughes (1997) supplemented
500 mg of calcium, as calcium citrate malate, and 17.5 micrograms
of vitamin D3 on top of a dietary calcium intake of 700 mg per day
and initial calcidiol levels of 75 nmol/l. Non-vertebral fractures
were reduced by 60% over three years. The effect on bone mineral
density change from the end of the first year to the end of the
third year was a reduction in loss of about 0.35% per year, similar
to the changes observed with calcium only.
supplementation with vitamin D alone appears to have no significant
effect on fracture risk, in general populations, despite a modest
reduction in bone loss (Lips, 1996; Peacock, 2000). The initial
calcidiol levels in Lips (1996) were 25 nmol/l, so the failure to
find a benefit is not explicable by higher initial levels of calcidiol.
This illustrates the importance of tackling fracture risk on a broad
front rather than relying on a single intervention.
evidence from intervention trials shows a benefit of increasing
calcium intake to between 1000 and 2000 mg per day, with a possible
further benefit on fracture rate by simultaneously ensuring adequate
vitamin D intake. Greater increases in calcium intake are not supported
by existing studies.
effects of calcium supplementation on bone mass and fracture risk
observed in intervention trials make a conclusive case for a benefit
states that "no further distinction need be made between dietary
and supplemental sources of calcium" but this assertion is
not well founded. The results of Recker (1985) discussed above indicate
that the effect of milk on calcium balance is about 70% of the effect
of its calcium content, as predicted by the model presented in Appendix
1. The model further predicts that not all dairy products are alike.
At moderate calcium intakes some cheeses make a modest positive
contribution to calcium balance while others make a negative contribution.
For individuals with relatively low calcium absorption, increased
consumption of cheese will generally cause a reduction in calcium
balance, so cheese cannot be expected to act as an effective source
of calcium. Milk and yoghurt are the only dairy products that are
likely to improve calcium balance on calcium intakes above 500mg
per day, though even they will be less effective than many other
sources of calcium.
There is only
one long term trial of increasing dairy product consumption. Baran
(1990) used unspecified dairy products to increase calcium consumption
from 900 mg per day to 1500 mg per day in premenopausal women. The
study showed a statistically significant difference in vertebral
bone density after 30 months. This was largely due to an apparent
3% drop in BMD in the unsupplemented control group between 18 months
and 30 months. Neither group showed any clear change in BMD during
any other time interval. This pattern does not allow evaluation
of the effect of the intervention after the remodelling transient
has ended as it suggests a higher degree of random error in the
measurements than indicated in the paper or some artefact such as
one or more women in the control group entering menopause: there
is no reason to expect premenopausal women to lose 3% of bone mineral
density in a year.
There are no
experimental data which contradict the expectation, based on the
model in Appendix 1, that increased milk consumption will show less
benefit than expected based on its calcium content and that increased
cheese consumption will show negligible benefit and may indeed have
a modest adverse effect on high risk individuals with relatively
low calcium absorption. Results from epidemiological observations
are consistent with this view. These results are discussed in more
detail in Appendix 3.
3: Epidemiological studies on dietary calcium and bone health
There is considerable
evidence from studies in Asia, such as Hirota (1992), Hu (1993),
Fujiwara (1997) and Lau (2001), that increasing calcium intake to
above 500 mg per day benefits bone health. It would be astonishing
if it did not. In many cases, the additional calcium is provided
by milk or other dairy products. Calcium intakes below 500 mg per
day are not consistent with optimal bone health in any society with
an ageing population. Such low calcium intakes will reduce bone
growth during childhood and adolescence, increasing the adverse
effect of later losses. Heaney (2000c) provides many other examples
of studies supporting this conclusion.
evidence short of intervention studies comes from prospective studies.
In prospective studies, the characteristics of healthy individuals
are recorded prior to observing their health over a number of years.
This avoids bias due to current diet and recollection of past diet
being altered by existing illness. However, such studies are still
subject to confounding by associations between different characteristics
of the same individual.
Cumming (1997) found a 50% increased risk of vertebral or hip fracture
in calcium supplement users. This observation contradicts the results
of the intervention trials discussed in Appendix 2. The results
were unlikely to be due to chance, so potential explanations need
to be considered. The obvious explanation is that individuals who
perceive themselves to be at high risk of fracture are more likely
to take calcium supplements than individuals with robust bone structure
and no family history of osteoporosis. The higher pre-existing risk
for such individuals then becomes associated with the use of calcium
supplements. Indeed, the authors found "supplement users were
more likely than were nonusers to have a history of falls, fractures
or osteoporosis" and considered this to be the most likely
explanation of the observed association. Cumming (1997) also found
a similar, but not statistically significant, association between
both dietary calcium and milk intake and vertebral fracture, which
may be subject to the same explanation.
found an increase of 200 mg of dietary calcium per 1000 kcal to
reduce fracture risk by 40%. This result is consistent with the
intervention studies discussed above.
Most other prospective
studies found no significant effect of dietary calcium. This may,
in part, reflect the difficulty of accurately measuring calcium
consumption. It may also reflect the expected difference in effect
between different sources of calcium. There is also likely to be
a variable degree of confounding due to high risk individuals choosing
to consume more dietary calcium.
(1997) found an adverse association between dietary calcium intake
and dairy calcium intake and risk of hip fracture. The highest quartile
of either dietary or dairy calcium intake showed a 100% increase
in risk of hip fracture compared with the lowest quartile. That
is, those individuals in the top 25% by calcium consumption had
a risk of fracture twice that of those in the bottom 25%. There
was also a tendency towards an adverse association between current
milk consumption and hip fracture rate, which was statistically
significant for consumption of three or more glasses of milk per
day (increased risk of 75%). Feskanich also found a tendency towards
a protective association from increased childhood milk consumption
(decreased risk of 47% for three or more glasses of milk per day)
and no change in risk associated with life-long high milk consumption.
The trend in
these results is as expected from the basic mechanics of calcium
balance set out in the present paper. That is, the benefit of a
high calcium intake is expected to be greatest in children and younger
adults, who show better absorption of calcium. The balance between
increased calcium intake and increased calcium losses with increased
dairy product consumption will thus be more favourable for them
than for older adults. The observation that milk consumption is
associated with a less pronounced adverse effect than overall dietary
calcium is also unsurprising. However, the apparent increase in
risk of fracture by a factor of two with high current dietary calcium
intake in older adults is not expected from the predicted effect
of dietary calcium sources on calcium balance, which only suggests
only a modest adverse impact of cheese in high risk individuals.
It is possible
that the Feskanich study was confounded by high risk individuals
choosing to drink milk and consume more dairy products in an attempt
to reduce risk. This is made more probable as the study was carried
out among nurses in the USA who would be well aware of conventional
risk factors for fracture and influenced by strong promotion of
dairy products as a protective measure. This effect of high risk
groups adopting behaviours believed to be protective is well established
and is the reason why the analysis in Feskanich (1997) was carried
out after eliminating calcium supplement users.
of the observed results is supported by analysing the results of
Feskanich (1998) which differentiated the same study population
based on a genetic risk factor for osteoporosis. Each hip fracture
case was matched with two controls with no fracture, and a genetic
test was carried out to unmask the genetic risk factor. The high
risk (BB) genetic subgroup had a twofold increase in hip fracture
risk compared with the other subgroups (Bb and bb). Elevated risk
of fracture was observed only in the BB group with low calcium intake
compared to other groups with low calcium intake.
presented in the paper were analysed further by reconstructing unpublished
data on the numbers of study members in each genetic group and calcium
intake level combination. This reconstruction is shown in Table
Table 5: Distribution of cases and controls by genotype and calcium
that 60% of the high genetic risk (BB) group were in the high calcium
intake group. The high risk individuals in the high calcium group
show a modest reduction in risk. That is, unmasking the hidden risk
factor indicates the expected modest protective effect of high dietary
calcium (-20%) rather than an apparent adverse effect when the entire
high calcium group is compared with the low calcium group (+50%).
This analysis shows that at least some of the apparent adverse effect
of dietary calcium is due to confounding by high risk individuals
choosing a behaviour believed to be protective. Indeed, it is possible
that a true protective effect of dietary calcium is being masked
by this confounding, though it is likely that any such effect is
modest compared with other risk factors.
It is also possible
that some factor in dairy products, other than their mineral and
protein content, is having an adverse effect. Melhus (1998) sheds
some light on this possibility. An analysis of fracture data in
a Swedish cohort, adjusting for multiple nutrients, showed an adverse
effect of calcium on fracture risk. However, Melhus noted an association
of fracture risk with intake of retinol (pre-formed vitamin A).
Compared with intakes of less than 500 micrograms per day, there
was a 30% increase in risk for intakes between 1000 and 1500 micrograms
per day and a 95% increase in risk for intakes above 1500 micrograms
per day. Adding retinol to the nutrients being considered eliminated
the elevated risk associated with high calcium intake. This did
not, however, eliminate milk consumption as a risk factor since
in Sweden low fat milk contains 450 micrograms of retinol per litre.
This study illustrates the fallacy of regarding milk as equivalent
to calcium. Milk contains many substances and cannot be assumed
to act simply as a calcium source
of high retinol intakes with osteoporosis was recently confirmed
in the USA (Feskanich, 2002). An 89% increase in risk of fracture
was observed for total retinol intakes of more than 2000 micrograms
per day compared with intakes of less than 500 micrograms. A 69%
increase in risk was found for retinol intakes from food above 1000
micrograms per day compared with less than 400 micrograms. Beta
carotene (converted in the body to vitamin A) was not associated
with excess risk in either Melhus (1998) or Feskanich (2002). The
consistency of results between Sweden and the USA, despite many
other differences between the two countries, strongly supports a
true adverse effect of retinol and the absence of any adverse effect
from plant carotenes.
have notably influenced the results in Feskanich (1997, 1998), as
US milk which has been fortified with vitamin A (the most common
sort) contains about 600 micrograms of retinol per litre compared
with 450 micrograms per litre in Swedish milk. While the USA does
not make extensive use of cod liver oil, which is a major source
of retinol in Scandinavia, there is extensive use of multivitamins
containing retinol. High consumption of milk fortified with vitamin
A will make a significant contribution to total retinol intake and
thus to the likelihood of consuming more than 1500 micrograms per
day, the apparent threshold for a notable adverse effect.
Trends in dairy
product consumption in the USA (Miller, 2000) may contribute strongly
to the difference between the results of Holbrook (1988) and Feskanich
(1997). Between 1970 and 1995, milk consumption declined from 320
ml per person per day to 240 ml per person per day. Whole milk consumption
declined by over 60%, while low fat milk consumption increased from
less than 20% to more than 60% of total milk consumption. Cheese
consumption increased from 13 g per person per day to 34 g per person
per day. Holbrook (1988) was based on a sample from a community
in California, aged 50 to 79 at the start of the study, over the
period 1973 to 1987. Feskanich (1997) was based on US nurses, aged
34 to 59 at the start of the study, over the period 1980 to 1992.
Differences in patterns of consumption of dairy products between
the two groups may have been greater than indicated by national
trends, due to differences in age and professional background.
Full fat milk
contains only about 200 micrograms of retinol per litre compared
with about 600 micrograms per litre in fortified low fat milk. The
analysis in the current paper also shows that for people at high
risk of osteoporosis due to relatively low calcium absorption cheese
will make calcium balance worse.
also provides an interesting insight into the complexity of the
effect of dietary calcium. High dietary calcium intake (>900
mg per day) was associated with a modest and non-significant increase
in bone loss at the spine (-0.48% compared with -0.35%) in postmenopausal
women who did not regularly use hormone replacement therapy (HRT).
In contrast, high calcium intake was associated with reduced bone
loss (+0.3% compared with -0.05%) in regular HRT users. As oestrogen
treatment makes calcium metabolism more like that of younger women,
this effect is consistent with the prediction in this paper that
the benefit of dairy products for bone health will diminish or even
reverse with age.
studies of dietary calcium are consistent with a protective effect
in childhood and adolescence which declines with age and may be
reversed, particularly for cheese, in older adults at high risk
for osteoporosis due to low calcium absorption. For older adults,
the addition of retinol to milk may introduce an increase in risk
greater than any benefit from the calcium provided.
4: Protein and bone health
between countries (Frassetto, 2000) indicate that an increase in
the ratio of animal to vegetable protein is strongly associated
with increased age-adjusted hip fracture rates in women over the
age of fifty. In the original 33 countries analysed, 70% of the
variation was explained by animal to vegetable protein ratio, but
the observed effect is likely to have been inflated by confounding.
The effect is
reduced when comparisons are restricted to 20 predominantly Caucasian
countries with female disability-adjusted life expectancy over 71,
but is still statistically significant (p=0.014) and explains 25%
of the variation of hip fracture incidence among these countries.
In the 20 country analysis carried out by Stephen Walsh, there was
no effect from total protein intake or disability-adjusted life
expectancy, but both were uniformly high (70 to 110 g protein per
person per day and 71 to 77 years life expectancy). In the Graph
1, age-adjusted hip fracture incidence is plotted against the ratio
of animal protein to vegetable protein (blue diamonds). The purple
squares indicate the best straight line fit obtained by regressing
hip fracture incidence against the ratio.
Graph 1: Inter-country comparison of hip fracture incidence and
ratio of animal to vegetable protein
association remained significant when the cluster of four countries
at the top right of the graph (Germany, Denmark, Sweden and Norway)
was eliminated from the analysis. Such comparisons between countries
are vulnerable to confounding, but the results are consistent with
a real benefit from consuming a higher proportion of protein from
vegetable sources while maintaining an adequate protein intake.
suggests that this association may reflect the effect of animal
and vegetable protein sources on net alkali consumption. This is
a possible factor, but many concentrated sources of vegetable protein,
such as soy and beans, have a positive impact on calcium balance
while meat, fish and eggs have a negative effect. Milk also has
a positive effect, albeit much less than that of kale and spring
greens. Some cheeses have a modestly positive effect, though the
positive effect of cheese disappears at higher overall calcium intakes.
The effect of different protein sources on calcium balance provides
a clear and direct explanation for the observed association, though
the balance between protein from milk and protein from other animal
sources would be expected to alter the observed effect of animal
It should be
emphasised that inadequate overall protein intakes can be expected
to adversely affect bone health. However, at any given protein intake
bone health is expected to be favoured by a high ratio of vegetable
to animal protein. This is exactly what was observed by Sellmeyer
(2001). Age-adjusted bone mineral density was positively associated
with the ratio of animal to vegetable protein, but on adjustment
for total protein intake and other factors the apparent relationship
was reversed, though this was not statistically significant. The
picture on hip fracture incidence was more straightforward, with
the age and weight adjusted risk of fracture rising with animal
protein intake and falling with vegetable protein intake. Bone loss
was observed to increase with increasing ratio of animal to vegetable
protein even before adjustment for total protein.
found a 25% increase in risk of forearm fracture as animal protein
intake rose from 50 g per day or less to 80 g per day or more. There
was no apparent effect of animal protein on hip fracture risk. Change
in vegetable protein intakes from less than 12 g per day to 20 g
per day or more showed no apparent effect.
only Sellmeyer (2001) and Feskanich (1996) gives a misleading impression
of the balance of evidence.
found reduced bone loss at the hip and spine over four years in
individuals in the highest quartile of animal protein intake, whether
measured in grams per day or as a percentage of calories. Kerstetter
(2000) found BMD of the femur to be 3.5% higher in the top quartile
of protein intake compared with the bottom quartile. No distinction
was made between animal and vegetable protein. Munger (1999) found
a 70% reduction in hip fracture risk in the highest quartile of
animal protein intake compared with vegetable protein intake.
reviews studies on protein intake and bone health up to 1998 noting
that 3 showed and adverse effect, three showed a beneficial effect
and two showed no significant effect. Heaney argues that the effect
of protein on bone will be modified substantially by the associated
ratio of calcium to protein, suggesting that there should be no
adverse effect of protein on bone if about 20 mg of calcium are
consumed for each gram of protein. That is, the effect of animal
protein will depend on the ratio of high calcium dairy products
to other animal protein sources. It is also likely that the effect
of protein will be different as protein intake increases to adequate
levels and then moves beyond such levels. There is some evidence
that protein requirements may be higher in older adults than in
younger adults (Hannan, 2001).
in an editorial on Sellmeyer (2001), argues that there is no valid
scientific reason for making a distinction between animal and vegetable
protein. Heaney notes correctly that grain protein is higher in
sulphur amino acids than many meat proteins. However, the concentrated
plant proteins that would be used to increase protein intake on
a vegan diet, such as soy products and beans, are relatively low
in sulphur amino acids. Moreover, other components of plant sources
of protein, particularly potassium and bicarbonate, also exert an
influence on calcium balance and, with the exception of grains,
this influence is markedly in favour of vegetable sources of protein.
on protein strongly supports an overall benefit for bone health
of higher protein intakes, provided a good calcium balance is maintained
and the diet is not excessively acidic. The ratio of animal to vegetable
protein does not adequately capture these provisos, so conflicting
results are to be expected. Replacing protein from meat, fish or
eggs with protein from milk or yoghurt will improve calcium balance.
Eliminating all animal proteins and living almost exclusively on
grains can be expected to be harmful. Replacing meat, fish or eggs
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My thanks to
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interests of clarity.